Genetic Analysis of a Morphological Shape Difference in the Male Genitalia of Drosophila simulans and D. mauritiana

INVESTIGATIONS

Genetic Analysis of a Morphological Shape Difference in the Male Genitalia of Drosophila simulans and D. mauritiana

J. Liu, J. M. Mercer, L. F. Stam, G. C. Gibson, Z. B. Zeng and C. C. Laurie
Department of Zoology, Duke University, Durham, North Carolina 27708

Two closely related species of Drosophila, D. simulans and D. mauritiana, differ markedly in morphology of the posterior lobe of the male genital arch. Both size and shape aspects of lobe variation can be quantified by a morphometric descriptor based on elliptical Fourier and principal components analyses. The genetic architecture of this quantitative trait (PC1) was investigated by hybridizing inbred lines to produce two backcross populations of ~200 individuals each, which were analyzed jointly by a composite interval mapping procedure with the aid of 18 marker loci. The parental lines show a large difference in PC1 (30.4 environmental standard deviations), and the markers account for >80% of the phenotypic variation in backcross populations. Eight of 15 intervals analyzed show convincing evidence of quantitative trait loci (QTL), and the range of estimated QTL effects is 5.7-15.9% of the parental difference (1.7-4.8 environmental standard deviations). These estimates may represent the joint effects of multiple QTL within a single interval (which averaged 23 cM in length). Although there is some evidence of partial dominance of mauritiana alleles and for epistasis, the pattern of inheritance is largely additive.

This article has been cited by other articles:

R. M. Graze, O. Barmina, D. Tufts, E. Naderi, K. L. Harmon, M. Persianinova, and S. V. Nuzhdin
New Candidate Genes for Sex-Comb Divergence Between Drosophila mauritiana and Drosophila simulans
Genetics, August 1, 2007; 176(4): 2561 - 2576.
[Abstract] [Full Text] [PDF]

A. J. Moehring, A. Llopart, S. Elwyn, J. A. Coyne, and T. F. C. Mackay
The Genetic Basis of Prezygotic Reproductive Isolation Between Drosophila santomea and D. yakuba Due to Mating Preference
Genetics, May 1, 2006; 173(1): 215 - 223.
[Abstract] [Full Text] [PDF]

M. C. Hall, C. J. Basten, and J. H. Willis
Pleiotropic Quantitative Trait Loci Contribute to Population Divergence in Traits Associated With Life-History Variation in Mimulus guttatus
Genetics, March 1, 2006; 172(3): 1829 - 1844.
[Abstract] [Full Text] [PDF]

J. M. Gleason, J.-M. Jallon, J.-D. Rouault, and M. G. Ritchie
Quantitative Trait Loci for Cuticular Hydrocarbons Associated With Sexual Isolation Between Drosophila simulans and D. sechellia
Genetics, December 1, 2005; 171(4): 1789 - 1798.
[Abstract] [Full Text] [PDF]

R. Mihaljevic, H. F. Utz, and A. E. Melchinger
No Evidence for Epistasis in Hybrid and Per Se Performance of Elite European Flint Maize Inbreds from Generation Means and QTL Analyses
Crop Sci., October 27, 2005; 45(6): 2605 - 2613.
[Abstract] [Full Text] [PDF]

D. J. Begun and H. A. Lindfors
Rapid Evolution of Genomic Acp Complement in the melanogaster Subgroup of Drosophila
Mol. Biol. Evol., October 1, 2005; 22(10): 2010 - 2021.
[Abstract] [Full Text] [PDF]

N. B. Langlade, X. Feng, T. Dransfield, L. Copsey, A. I. Hanna, C. Thebaud, A. Bangham, A. Hudson, and E. Coen
Evolution through genetically controlled allometry space
PNAS, July 19, 2005; 102(29): 10221 - 10226.
[Abstract] [Full Text] [PDF]

K. Weber, N. Johnson, D. Champlin, and A. Patty
Many P-Element Insertions Affect Wing Shape in Drosophila melanogaster
Genetics, March 1, 2005; 169(3): 1461 - 1475.
[Abstract] [Full Text] [PDF]

A. J. Moehring, J. Li, M. D. Schug, S. G. Smith, M. deAngelis, T. F. C. Mackay, and J. A. Coyne
Quantitative Trait Loci for Sexual Isolation Between Drosophila simulans and D. mauritiana
Genetics, July 1, 2004; 167(3): 1265 - 1274.
[Abstract] [Full Text] [PDF]

J. M. Gleason and M. G. Ritchie
Do Quantitative Trait Loci (QTL) for a Courtship Song Difference Between Drosophila simulans and D. sechellia Coincide With Candidate Genes and Intraspecific QTL?
Genetics, March 1, 2004; 166(3): 1303 - 1311.
[Abstract] [Full Text] [PDF]

Y. Tao, S. Chen, D. L. Hartl, and C. C. Laurie
Genetic Dissection of Hybrid Incompatibilities Between Drosophila simulans and D. mauritiana. I. Differential Accumulation of Hybrid Male Sterility Effects on the X and Autosomes
Genetics, August 1, 2003; 164(4): 1383 - 1397.
[Abstract] [Full Text] [PDF]

Y. Tao, Z.-B. Zeng, J. Li, D. L. Hartl, and C. C. Laurie
Genetic Dissection of Hybrid Incompatibilities Between Drosophila simulans and D. mauritiana. II. Mapping Hybrid Male Sterility Loci on the Third Chromosome
Genetics, August 1, 2003; 164(4): 1399 - 1418.
[Abstract] [Full Text] [PDF]

H. Lan, J. P. Stoehr, S. T. Nadler, K. L. Schueler, B. S. Yandell, and A. D. Attie
Dimension Reduction for Mapping mRNA Abundance as Quantitative Traits
Genetics, August 1, 2003; 164(4): 1607 - 1614.
[Abstract] [Full Text] [PDF]

H. Iwata and Y. Ukai
SHAPE: A Computer Program Package for Quantitative Evaluation of Biological Shapes Based on Elliptic Fourier Descriptors
J. Hered., September 1, 2002; 93(5): 384 - 385.
[Full Text] [PDF]

M. S. Workman, L. J. Leamy, E. J. Routman, and J. M. Cheverud
Analysis of Quantitative Trait Locus Effects on the Size and Shape of Mandibular Molars in Mice
Genetics, April 1, 2002; 160(4): 1573 - 1586.
[Abstract] [Full Text] [PDF]

K. Weber, R. Eisman, S. Higgins, L. Morey, A. Patty, M. Tausek, and Z.-B. Zeng
An Analysis of Polygenes Affecting Wing Shape on Chromosome 2 in Drosophila melanogaster
Genetics, November 1, 2001; 159(3): 1045 - 1057.
[Abstract] [Full Text] [PDF]

Y. Tao, D. L. Hartl, and C. C. Laurie
Sex-ratio segregation distortion associated with reproductive isolation in Drosophila
PNAS, October 25, 2001; (2001) 231478798.
[Abstract] [Full Text] [PDF]

C.-T. Ting, A. Takahashi, and C.-I Wu
Incipient speciation by sexual isolation in Drosophila: Concurrent evolution at multiple loci
PNAS, June 5, 2001; 98(12): 6709 - 6713.
[Abstract] [Full Text] [PDF]

C. P. Klingenberg, L. J. Leamy, E. J. Routman, and J. M. Cheverud
Genetic Architecture of Mandible Shape in Mice: Effects of Quantitative Trait Loci Analyzed by Geometric Morphometrics
Genetics, February 1, 2001; 157(2): 785 - 802.
[Abstract] [Full Text]

S. P. Otto and C. D. Jones
Detecting the Undetected: Estimating the Total Number of Loci Underlying a Quantitative Trait
Genetics, December 1, 2000; 156(4): 2093 - 2107.
[Abstract] [Full Text]

V. L. Roth and J. M. Mercer
Morphometrics in Development and Evolution
Integr. Comp. Biol., October 1, 2000; 40(5): 801 - 810.
[Abstract] [Full Text] [PDF]

T. Takano-Shimizu
Genetic Screens for Factors Involved in the Notum Bristle Loss of Interspecific Hybrids Between Drosophila melanogaster and D. simulans
Genetics, September 1, 2000; 156(1): 269 - 282.
[Abstract] [Full Text]

E. Zimmerman, A. Palsson, and G. Gibson
Quantitative Trait Loci Affecting Components of Wing Shape in Drosophila melanogaster
Genetics, June 1, 2000; 155(2): 671 - 683.
[Abstract] [Full Text]

Z.-B. Zeng, J. Liu, L. F. Stam, C.-H. Kao, J. M. Mercer, and C. C. Laurie
Genetic Architecture of a Morphological Shape Difference Between Two Drosophila Species
Genetics, January 1, 2000; 154(1): 299 - 310.
[Abstract] [Full Text]

D. W. Schemske and H. D. Bradshaw Jr.
Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus)
PNAS, October 12, 1999; 96(21): 11910 - 11915.
[Abstract] [Full Text] [PDF]

R. L. Wu
Mapping Quantitative Trait Loci by Genotyping Haploid Tissues
Genetics, August 1, 1999; 152(4): 1741 - 1752.
[Abstract] [Full Text]

U. Bhadra, M. P. Bhadra, and J. A. Birchler
Interactions Among Dosage-Dependent Trans-Acting Modifiers of Gene Expression and Position-Effect Variegation in Drosophila
Genetics, September 1, 1998; 150(1): 251 - 263.
[Abstract] [Full Text]

C. D. Jones
The Genetic Basis of Drosophila sechellia's Resistance to a Host Plant Toxin
Genetics, August 1, 1998; 149(4): 1899 - 1908.
[Abstract] [Full Text] [PDF]

T. S. Takano
Loss of Notum Macrochaetae as an Interspecific Hybrid Anomaly Between Drosophila melanogaster and D. simulans
Genetics, July 1, 1998; 149(3): 1435 - 1450.
[Abstract] [Full Text] [PDF]

H. D. Bradshaw , Jr., K. G. Otto, B. E. Frewen, J. K. McKay, and D. W. Schemske
Quantitative Trait Loci Affecting Differences in Floral Morphology Between Two Species of Monkeyflower (Mimulus)
Genetics, May 1, 1998; 149(1): 367 - 382.
[Abstract] [Full Text] [PDF]

S. R. Voss and H. B. Shaffer
Adaptive evolution via a major gene effect: Paedomorphosis in the Mexican axolotl
PNAS, December 9, 1997; 94(25): 14185 - 14189.
[Abstract] [Full Text] [PDF]

Y. Tao, D. L. Hartl, and C. C. Laurie
Sex-ratio segregation distortion associated with reproductive isolation in Drosophila
PNAS, November 6, 2001; 98(23): 13183 - 13188.
[Abstract] [Full Text] [PDF]

				A. J. Moehring, A. Llopart, S. Elwyn, J. A. Coyne, and T. F. C. Mackay The Genetic Basis of Prezygotic Reproductive Isolation Between Drosophila santomea and D. yakuba Due to Mating Preference Genetics, May 1, 2006; 173(1): 215 - 223. [Abstract] [Full Text] [PDF]

				M. C. Hall, C. J. Basten, and J. H. Willis Pleiotropic Quantitative Trait Loci Contribute to Population Divergence in Traits Associated With Life-History Variation in Mimulus guttatus Genetics, March 1, 2006; 172(3): 1829 - 1844. [Abstract] [Full Text] [PDF]

				J. M. Gleason, J.-M. Jallon, J.-D. Rouault, and M. G. Ritchie Quantitative Trait Loci for Cuticular Hydrocarbons Associated With Sexual Isolation Between Drosophila simulans and D. sechellia Genetics, December 1, 2005; 171(4): 1789 - 1798. [Abstract] [Full Text] [PDF]

				R. Mihaljevic, H. F. Utz, and A. E. Melchinger No Evidence for Epistasis in Hybrid and Per Se Performance of Elite European Flint Maize Inbreds from Generation Means and QTL Analyses Crop Sci., October 27, 2005; 45(6): 2605 - 2613. [Abstract] [Full Text] [PDF]

				D. J. Begun and H. A. Lindfors Rapid Evolution of Genomic Acp Complement in the melanogaster Subgroup of Drosophila Mol. Biol. Evol., October 1, 2005; 22(10): 2010 - 2021. [Abstract] [Full Text] [PDF]

				N. B. Langlade, X. Feng, T. Dransfield, L. Copsey, A. I. Hanna, C. Thebaud, A. Bangham, A. Hudson, and E. Coen Evolution through genetically controlled allometry space PNAS, July 19, 2005; 102(29): 10221 - 10226. [Abstract] [Full Text] [PDF]

				K. Weber, N. Johnson, D. Champlin, and A. Patty Many P-Element Insertions Affect Wing Shape in Drosophila melanogaster Genetics, March 1, 2005; 169(3): 1461 - 1475. [Abstract] [Full Text] [PDF]

				A. J. Moehring, J. Li, M. D. Schug, S. G. Smith, M. deAngelis, T. F. C. Mackay, and J. A. Coyne Quantitative Trait Loci for Sexual Isolation Between Drosophila simulans and D. mauritiana Genetics, July 1, 2004; 167(3): 1265 - 1274. [Abstract] [Full Text] [PDF]

				J. M. Gleason and M. G. Ritchie Do Quantitative Trait Loci (QTL) for a Courtship Song Difference Between Drosophila simulans and D. sechellia Coincide With Candidate Genes and Intraspecific QTL? Genetics, March 1, 2004; 166(3): 1303 - 1311. [Abstract] [Full Text] [PDF]

				Y. Tao, S. Chen, D. L. Hartl, and C. C. Laurie Genetic Dissection of Hybrid Incompatibilities Between Drosophila simulans and D. mauritiana. I. Differential Accumulation of Hybrid Male Sterility Effects on the X and Autosomes Genetics, August 1, 2003; 164(4): 1383 - 1397. [Abstract] [Full Text] [PDF]

				Y. Tao, Z.-B. Zeng, J. Li, D. L. Hartl, and C. C. Laurie Genetic Dissection of Hybrid Incompatibilities Between Drosophila simulans and D. mauritiana. II. Mapping Hybrid Male Sterility Loci on the Third Chromosome Genetics, August 1, 2003; 164(4): 1399 - 1418. [Abstract] [Full Text] [PDF]

				H. Lan, J. P. Stoehr, S. T. Nadler, K. L. Schueler, B. S. Yandell, and A. D. Attie Dimension Reduction for Mapping mRNA Abundance as Quantitative Traits Genetics, August 1, 2003; 164(4): 1607 - 1614. [Abstract] [Full Text] [PDF]

				H. Iwata and Y. Ukai SHAPE: A Computer Program Package for Quantitative Evaluation of Biological Shapes Based on Elliptic Fourier Descriptors J. Hered., September 1, 2002; 93(5): 384 - 385. [Full Text] [PDF]

				M. S. Workman, L. J. Leamy, E. J. Routman, and J. M. Cheverud Analysis of Quantitative Trait Locus Effects on the Size and Shape of Mandibular Molars in Mice Genetics, April 1, 2002; 160(4): 1573 - 1586. [Abstract] [Full Text] [PDF]

				K. Weber, R. Eisman, S. Higgins, L. Morey, A. Patty, M. Tausek, and Z.-B. Zeng An Analysis of Polygenes Affecting Wing Shape on Chromosome 2 in Drosophila melanogaster Genetics, November 1, 2001; 159(3): 1045 - 1057. [Abstract] [Full Text] [PDF]

				Y. Tao, D. L. Hartl, and C. C. Laurie Sex-ratio segregation distortion associated with reproductive isolation in Drosophila PNAS, October 25, 2001; (2001) 231478798. [Abstract] [Full Text] [PDF]

				C.-T. Ting, A. Takahashi, and C.-I Wu Incipient speciation by sexual isolation in Drosophila: Concurrent evolution at multiple loci PNAS, June 5, 2001; 98(12): 6709 - 6713. [Abstract] [Full Text] [PDF]

				C. P. Klingenberg, L. J. Leamy, E. J. Routman, and J. M. Cheverud Genetic Architecture of Mandible Shape in Mice: Effects of Quantitative Trait Loci Analyzed by Geometric Morphometrics Genetics, February 1, 2001; 157(2): 785 - 802. [Abstract] [Full Text]

				S. P. Otto and C. D. Jones Detecting the Undetected: Estimating the Total Number of Loci Underlying a Quantitative Trait Genetics, December 1, 2000; 156(4): 2093 - 2107. [Abstract] [Full Text]

				V. L. Roth and J. M. Mercer Morphometrics in Development and Evolution Integr. Comp. Biol., October 1, 2000; 40(5): 801 - 810. [Abstract] [Full Text] [PDF]

				T. Takano-Shimizu Genetic Screens for Factors Involved in the Notum Bristle Loss of Interspecific Hybrids Between Drosophila melanogaster and D. simulans Genetics, September 1, 2000; 156(1): 269 - 282. [Abstract] [Full Text]

				E. Zimmerman, A. Palsson, and G. Gibson Quantitative Trait Loci Affecting Components of Wing Shape in Drosophila melanogaster Genetics, June 1, 2000; 155(2): 671 - 683. [Abstract] [Full Text]

				Z.-B. Zeng, J. Liu, L. F. Stam, C.-H. Kao, J. M. Mercer, and C. C. Laurie Genetic Architecture of a Morphological Shape Difference Between Two Drosophila Species Genetics, January 1, 2000; 154(1): 299 - 310. [Abstract] [Full Text]

				D. W. Schemske and H. D. Bradshaw Jr. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus) PNAS, October 12, 1999; 96(21): 11910 - 11915. [Abstract] [Full Text] [PDF]

				R. L. Wu Mapping Quantitative Trait Loci by Genotyping Haploid Tissues Genetics, August 1, 1999; 152(4): 1741 - 1752. [Abstract] [Full Text]

				U. Bhadra, M. P. Bhadra, and J. A. Birchler Interactions Among Dosage-Dependent Trans-Acting Modifiers of Gene Expression and Position-Effect Variegation in Drosophila Genetics, September 1, 1998; 150(1): 251 - 263. [Abstract] [Full Text]

				C. D. Jones The Genetic Basis of Drosophila sechellia's Resistance to a Host Plant Toxin Genetics, August 1, 1998; 149(4): 1899 - 1908. [Abstract] [Full Text] [PDF]

				T. S. Takano Loss of Notum Macrochaetae as an Interspecific Hybrid Anomaly Between Drosophila melanogaster and D. simulans Genetics, July 1, 1998; 149(3): 1435 - 1450. [Abstract] [Full Text] [PDF]

				H. D. Bradshaw , Jr., K. G. Otto, B. E. Frewen, J. K. McKay, and D. W. Schemske Quantitative Trait Loci Affecting Differences in Floral Morphology Between Two Species of Monkeyflower (Mimulus) Genetics, May 1, 1998; 149(1): 367 - 382. [Abstract] [Full Text] [PDF]

				S. R. Voss and H. B. Shaffer Adaptive evolution via a major gene effect: Paedomorphosis in the Mexican axolotl PNAS, December 9, 1997; 94(25): 14185 - 14189. [Abstract] [Full Text] [PDF]